Black Rats, Island Characteristics, and Colonial Nesting Birds in the Mediterranean: Consequences of an Ancient Introduction JEAN-LOUIS MARTIN,*§ JEAN-CLAUDE THIBAULT,† AND VINCENT BRETAGNOLLE‡ *Centre d’Ecologie Fonctionnelle et Evolutive/Centre Nacional de la Recherche Scientifique, 1919 route de Mende, F-34293 Montpellier Cedex 5, France †Parc Naturel Régional de Corse, rue Major Lambroschini, B.P. 417, F-20184 Ajaccio, Corsica ‡Centre d’Etudes Biologiques de Chizé/Centre Nacional de la Recherche Scientifique 4701, F-79360 Beauvoir-sur-Niort Abstract: The devastation of island faunas by alien species has been instrumental in raising concerns about the global threat to biological diversity. Colonial nesting species, often restricted to islands, have been affected severely. Eradication of introduced species as a means to alleviate the problem is usually done with little or no understanding of the mechanisms governing interactions between introduced and native species. Such an understanding could help target management action. We analyzed how island area, rock substrate, bird spe- cies biology, and presence of an introduced species, the black rat ( Rattus rattus), interact to explain the distri- bution and abundance of colonial nesting birds on a set of 72 islands from six archipelagos in the western Mediterranean. Rats were introduced to this region over 2000 years ago, and these communities have had time to reach an equilibrium. Using general linear models, we show that rats have affected species distribu- tions more on the smaller islands and on islands with an acidic or neutral rock substrate; larger bird species are more resistant. On the smaller islands, where rat densities are highest, larger colonial birds are negatively affected. On larger islands, where rat densities are lower and fluctuate form year to year, larger colonial birds can maintain healthy populations despite the presence of rats. Although rats caused local extinction or reduc- tion in bird abundance, the presence of islands varying in size and/or substrate allowed most archipelagos to retain their suite of colonial nesting bird species, despite a presumably reduced abundance for most species. Ratas Negras, Características de Islas, y Nidación Colonial de Aves en el Mediterráneo: Consecuencias de una Introducción Ancestral Resumen: La devastación de las faunas isleñas por especies forasteras ha sido instrumental en lo que re- specta a elevar preocupaciones sobre la amenaza global contra la diversidad biológica. Las especies de ni- dación colonial, frecuentemente restringidas a islas, han sido severamente afectadas. La erradicación de es- pecies introducidas como un medio para aliviar el problema es generalmente realizada con poco o ningún entendimiento de los mecanismos que gobiernan las interacciones entre las especies nativas y las introduci- das. Este tipo de entendimiento podría ayudar a enfocar medidas de manejo. Nosotros analizamos como el área, el substrato rocoso, la biología de la especie de ave, y la presencia de una especie introducida, la rata negra ( Rattus rattus), interactúan para explicar la distribución y abundancia de aves con nidación colonial en 72 islas de seis archipiélagos en el Mediterráneo occidental. Las ratas fueron introducidas a esta región hace más de 2000 años y estas comunidades han tenido tiempo suficiente para alcanzar un equilibrio. Medi- ante el uso de modelos lineales generales mostramos que las ratas han afectado más la distribución de espe- cies en las islas pequeñas y en las islas grandes con un substrato rocoso ácido o neutro (textura burda), que en aquellas islas con caliza y textura fina. Las especies de aves más pequeñas son más sensibles a las ratas, más frecuentemente ausentes de las islas con ratas y sistemáticamente ausentes de islas con ratas y un sub- strato rocoso de estructura burda. Las especies de aves más grandes son más resistentes. En las islas más pe- §email [email protected] Paper submitted April 13, 1999; revised manuscript accepted January 5, 2000. 1452 Conservation Biology, Pages 1452–1466 Volume 14, No. 5, October 2000 Martin et al. Rats and Birds on Mediterranean Islands 1453 queñas, donde la densidad de las ratas es mayor, las aves coloniales grandes son afectadas negativamente. En islas más grandes, donde las densidades de ratas son menores, y fluctúan de un año al otro, las aves colo- niales grandes pueden mantener poblaciones saludables a pesar de la presencia de las ratas. No obstante que las ratas causaron extinciones locales o reducciones en la abundancia de aves, la presencia de islas que varían en tamaño y/o substrato permite que la mayoría de los archipiélagos mantengan su grupo de espe- cies de aves de nidación colonial, a pesar de una presumiblemente reducida abundancia en la mayoría de las especies. Introduction have been invaded much more recently. We focused on colonial nesting species, which are prey of high poten- Since Darwin and Wallace, patterns of species distribu- tial benefit to rats. We considered colonial nesting spe- tion on islands have been the subject of considerable at- cies as those species that nest in aggregated clumps and tention and have led to major advances in ecology and do not exhibit helping behavior (e.g., Wittenberger & biogeography (e.g., MacArthur & Wilson 1967; Lack Hunt 1985; Brown & Brown 1996). On these islands, co- 1976). More recently, the devastation of island ecosys- lonial nesting birds span a range of body size and taxa tems by introduced species has been instrumental in that can help in understanding the relationships among raising awareness of the global threat that human-driven predation risk, prey size, and prey biology. We also used dispersal of species is posing to biological diversity experimental analysis to assess interaction between rats (Bright 1998). Islands are essential for many species, es- and two colonial bird species on these islands (Thibault pecially for colonial nesting birds. On islands the latter 1995; Penloup et al. 1997). We tested four predictions: can find a combination of suitable habitats (e.g., Lack (1) the risk of extirpation by rats decreases with increas- 1968; Ashmole 1971; Ricklefs 1990) and the absence of ing prey body size; (2) for larger species, the presence of predators (including humans; review in Burger & Goch- rats affects population size in a density-dependent man- feld 1994). Indeed, the introduction of alien predators ner; (3) independent of prey body size, the effects of on islands has led to the extinction of numerous animal rats on distribution and abundance of cavity nesters de- populations (Atkinson 1996; for Mediterranean beetles, pends on island area, and (4) on substrate through varia- Palmer & Pons 1996), including colonial species (Atkin- tion in the availability of breeding sites safe from rats. son 1985; Collar et al. 1994). Rats (Polynesian, Rattus exulans; black, R. rattus; and Norway, R. norvegicus) have been among the first and most successful predators introduced to oceanic islands by Current Regional Geography of Rats and Colonial humans. Their impact, notably on colonial birds, has been Nesting Birds enormous (Moors & Atkinson 1984; Moors et al. 1992). Significant efforts to restore island ecosystems through The western Mediterranean basin spreads from Gibraltar rat eradication have been made and are continuing in to the Sicily channel ( Fig. 1). It covers about one-third of several archipelagos (e.g., Taylor & Thomas 1989; 1993; the 2.9 million km2 of the Mediterranean Sea, and it in- Chapuis et al. 1994; Siorat & Pascal 1995; Kaiser et al. cludes several hundred islands and islets. Of those, 471 1997). In contrast to these efforts, only moderate atten- occur around the Balearics, Corsica, Sardinia, and off- tion has been paid to understanding how introduced shore Provence, France. The black rat, native to eastern rats actually interact with native species. When and why Asia, reached Palestine around 3000 B.P. (Tchernov will certain species go extinct, decline, or persist in the 1986). Evidence of rats in the western Mediterranean presence of rats? What will be the long-term effect of the has been found on Corsica dating to 2400 B.P. (Vigne & alien species on the indigenous community? How is this Valladas 1996). At that time most of the islands sur- effect influenced by island characteristics? rounding Corsica and Sardinia were already separated We analyzed how black rats affect the distribution and from one another by the sea rise that followed the last abundance of colonial birds on islands of the western glacial period (van Andel 1990; Laborel et al. 1994). On Mediterranean. Current rat distribution in the Mediterra- Menorca, records date to 2200 B.P. (Reumer 1986), and nean is well documented, and reliable information exists on Zembra, Tunisia, to the fifth or sixth century A.D. on the time of colonization (Audouin-Rouzeau & Vigne (Vigne 1988). Sanges and Alcover (1980) found rat 1994). The introduction of the black rat to this region at bones on Sardinia in layers dating to 5500 B.P., but this least 2000 years ago makes it of special interest because date is still under debate (Audouin-Rouzeau & Vigne it is likely that the invaded communities have reached 1994). Only a few islands are close enough to the main some level of equilibrium. This is not necessarily the islands to be accessible by natural dispersal (Cheylan case in many of the isolated islands or archipelagos that 1986a), and the colonization process was probably de- Conservation Biology Volume 14, No. 5, October 2000 1454 Rats and Birds on Mediterranean Islands Martin et al. the Balearic or Tyrrhenian Sea), whereas the Audouin’s Gull (Larus audouinii ) breeds mainly in the Alboran Sea (east of Gibraltar), although it has recently colonized the Balearic Sea (Oro & Martinez-Vilalta 1992). Cory’s Shear- water (Calonectris diomedea) has a wide distribution and gathers in large colonies in relatively open seas (such as the central and southern Mediterranean), as does the Storm Petrel (Hydrobates pelagicus) but usually in smaller colonies (Zotier et al.